Hydraulic resistance components of mature apple trees on rootstocks of different vigours

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1 Journl of Experimentl Botny, Vol. 58, No. 15/16, pp , 2007 doi: /jxb/erm281 This pper is vilble online free of ll ccess chrges (see for further detils) RESEARCH PAPER Hydrulic resistnce components of mture pple trees on rootstocks of different vigours Shbti Cohen 1, *, Amos Nor 2, John Bennink 3, Avrhm Grv 1 nd Melvin Tyree 3,4 1 Institute of Soil, Wter nd Environmentl Sciences, ARO, POB 6, Bet Dgn 50250, Isrel 2 Goln Reserch Institute, POB 97, Kzrin 12900, Isrel 3 Northestern Reserch Sttion, USDA Forest Service, 705 Sper St, S. Burlington, VT 05403, USA 4 Deprtment of Renewble Resources, 444 Erth Sciences Building, University of Albert, Edmonton, AB, Cnd T6G 2E3 Received 12 July 2006; Revised 8 July 2007; Accepted 22 October 2007 Abstrct Dwrfing of fruit trees is often chieved through the use of dwrfing rootstocks. Dwrf trees re chrcterized by sustined reductions in vegettive growth during the lifetime of the tree. The dwrfing mechnism is not well understood, but it hs been hypothesized tht hydrulic properties of the rootstock nd the grft union re involved. It is hypothesized here tht lef- or stem-specific resistnce of t lest one hydrulic component of the wter trnsport system would be negtively correlted with rootstock vigour, nd this could be useful for selection of rootstocks. Hydrulic resistnce (R) of fully grown pple trees on vriety of rootstocks of different vigours ws mesured. Most mesurements were with the evportive flux (EF) method, where wter uptke mesured with sp flow sensors ws relted to the pressure grdient from soil (tken s pre-dwn lef) nd middy root (tken s covered root-sucker), stem (from covered lef), nd exposed nd shded lef wter potentils (W l ). R of trees on dwrfing M9 rootstock ws compred with tht of more vigorous MM106 nd MM111 rootstocks in Isrel nd Vermont, USA. In Isrel, M9 consistently hd higher lef-specific hydrulic resistnce (R l ) in the soil to scion stem pthwy, but this difference ws only significnt for one summer. R ws lrger in M9 between the root nd stem, implicting the grft union s the site of incresed resistnce. In Vermont, R l of 9- nd 10-yer-old trees on six rootstocks of vrious vigours ws not consistently relted to vigour, nd stem-specific resistnce (R s ) incresed with incresing vigour. High pressure flow meter (HPFM) mesurements gve lower R thn the EF method in ll but one cse, perhps indicting significnt mount of xylem dysfunction in these trees, nd demonstrted the incresed resistivity of stem sections tht included dwrf grft unions s compred with non-grft stem sections. It is concluded tht stem- nd lef-specific R re not consistently positively correlted with dwrfing, lthough the incresed resistivity of the grft union in dwrfing rootstocks my influence the trnsport of wter nd other elements cross the grft union, nd therefore be involved in the dwrfing mechnism. Key words: Conductnce, dwrfing, grft union, Mlus domestic, scion. Introduction Rootstocks cn bestow specific properties on the tree. One of the more importnt properties in modern orchrds is sustined reduction in vegettive growth rtes, or dwrfing. Severl studies hve hypothesized tht dwrfing by rootstocks results from n increse in lef-specific hydrulic resistnce (R l ), which cuses reductions in cnopy wter sttus nd in rtes of gs exchnge nd subsequent growth (Kmboj et l., 1997) or chnges in diurnl wter potentil vritions tht re relted to shoot elongtion (Bsile et l., 2003). There is prcticl importnce to this hypothesis, since breeders would like to be ble to determine rootstock s vigour from physiologicl prmeters, insted of rduous long-term trils. * To whom correspondence should be ddressed. E-mil: vwshep@gri.gov.il ª 2007 The Author(s). This is n Open Access rticle distributed under the terms of the Cretive Commons Attribution Non-Commercil License ( which permits unrestricted non-commercil use, distribution, nd reproduction in ny medium, provided the originl work is properly cited. Downloded from

2 4214 Cohen et l. Studies of dwrfing rootstocks in pple trees hve found evidence for incresed R (Olien nd Lkso, 1984, 1986; Higgs nd Jones, 1990). Mesurements hve shown tht sites of incresed R my be the root system (Syvertsen, 1981, for citrus; Bsile et l., 2003b, for pech; Nrdini et l., 2006, for olive) or the grft union region (Cohen nd Nor, 2002; Atkinson et l., 2003, for pples; Olmsted et l., 2006, for cherry). Apple nd pome fruit studies tht ctully mesured R ech trgeted only two or three rootstocks, nd no informtion is vilble on other rootstocks. In ddition, Cohen nd Nor (2002) were not ble to mesure the grft union region, nd Atkinson et l. (2003) mesured only few prts of young plnts. These deficiencies leve room for more focused study. R expresses the wter potentil (W) grdient necessry to cuse unit wter flux. Since the size of the W grdient is limited to potentils tht mintin the integrity of the wter columns in the xylem, R nd the mximum W grdient define the mximum rte of wter trnsport in the tree. This rte lso determines wht mximum lef conductnce to wter vpour nd CO 2 uptke cn be ttined for given mount of lef re. Thus, for given lef re nd W grdient, tree gs exchnge is limited by R. There is more thn one possibility for n influence of R nd its reciprocl, conductnce, on growth rtes of the scion. One direct mechnism is vi gs exchnge nd subsequent productivity. Such mechnism, nd the theoreticl connection between R l, cnopy conductnce, nd photosynthesis, hs been discussed elsewhere (Sperry, 2000; Cohen nd Nor, 2002). Cohen nd Nor (2002) found tht differences in lef-specific hydrulic conductnce between vigorous nd wek rootstocks were ccompnied by differences in cnopy conductnce, but no consistent differences in porometer mesurements of lef conductnce or crbon 13 isotopic rtios were found (Cohen et l., 2003). Similrly, Clerwter et l. (2004) did not find direct reltionship between dwrfing nd whole plnt hydrulic conductnce, wter sttus, nd photosynthesis in vigour-controlling kiwifruit (genus Actinidi) rootstocks. Nrdini et l. (2006) compred one dwrfing with one vigorous rootstock in olive trees nd found tht the reduced totl hydrulic conductnce of the root system of the dwrfing rootstock ws comprble with the reduction in lef re of the scion even though differences in lef-specific resistnce were minor. They concluded tht in this cse hydrulics could explin dwrfing, since the cnopy size ws coupled to root conductnce. Gsco et l. (2007), working with the sme olive rootstocks, found tht the resistnce of the grft union comprises significnt prt of the totl resistnce only during the first 2 months. Thus, sustined differences in scion vegettive growth could not be explined by differences in the grft union. Clerwter et l. (2006) found tht kiwifruit dwrfing is relted to differences in erly seson cnopy development, nd suggested tht differences in hydrulic conductnce t tht time my led to dwrfing, while most evlutions of hydrulic conductnce hve been mde fter full cnopy development. Another proposed mechnism for the hydrulic influence of rootstocks is tht diurnl vritions in stem wter potentil modulte stem elongtion (Bsile et l., 2003b). The ltter ws bsed on the correltion between the rte of chnge of wter potentil nd stem extension rte in pech trees, s investigted nd modelled by Bermn nd DeJong (1997). In ddition to restriction of wter trnsport, incresed R or differences in xylem properties my influence trnsport of solutes, including nutrients nd hormones in the xylem (Lockrd nd Schneider, 1981). Such influences might be considered to be indirect influences of chnges in R. Nonhydrulic mechnisms for dwrfing hve lso been suggested (Lockrd nd Schneider, 1981). Severl methods hve been used to mesure R in trees. All involve mesurement of pressure grdient nd the resulting flow rte. The evportive flux (EF) method determines R in vivo. For this method, sp flux nd W grdients re monitored. Sp flux nd W vry during the dy, so ssuming tht R chnges little during the dy the verge totl R might be determined from the liner reltionship between sp flux nd W (Pssiour nd Munns, 1984). However, cpcitnce of the tree, which in lrge pple trees cn mount to 2 h worth of trnspirtion (Lndsberg et l., 1976), cuses hysteresis in the reltionship, nd inccurcies when W is chnging (Moreshet et l., 1990). Nevertheless in summer cler sky conditions, middy sp flux nd wter potentil re usully constnt for severl hours t middy (Cohen nd Nor, 2002; Li et l., 2002), indicting stedy-stte flow nd no cpcitnce contribution to the EF t tht time. If W t different points in the soil root stem lef continuum is mesured t these times, then R cn be determined nd prtitioned (Moreshet et l., 1990). For totl plnt R, either lef W vlue corresponding to soil plnt equilibrium t zero flow or the soil wter potentil is needed (i.e. the intercept). The former is the cse before dwn, nd pre-dwn lef W hs been shown for citrus to be close to the zero intercept of the plot of W on sp flow (Cohen et l., 1983). For these resons, in the current study the pre-dwn lef W ws tken s proxy for soil W, which for non-dry soil ws ssumed to remin constnt during the dy. Additionl points used for prtitioning R re stem W, tken from mesurements of covered leves (Nor et l., 1995; Jones, 2004), nd lrge root W, tken from covered leves on root suckers (Simonneu nd Hbib, 1991). A direct R mesurement technique is with high pressure flow meter (HPFM; Tyree et l., 1995), in which the plnt is severed t point where pressure-tight connector cn be ttched, nd pressurized wter is forced into the plnt while the flow rte is monitored simultneously. In mny cses, this method gives results Downloded from

3 comprble with those obtined with the EF method (Tsud nd Tyree, 2000). This method is direct, nd cn be pplied in the field (Bsile et l., 2003b), but the pressure pplied is enough to hydrte nd ctivte dysfunctionl xylem (Sperry et l., 1988), so tht the results my underestimte the opertionl resistnce, giving potentil resistnce. EF R cn be severl times lrger thn tht obtined with the HPFM, nd the difference my give insight into the extent of cvittion nd/or xylem dysfunction (Rieger, 1989). This study investigtes the hypothesis tht stem- nd lef-specific R re correlted with sustined rootstock vigour. A series of field experiments were conducted to determine R of full-sized pple (Mlus domestic Borkh.) trees on seven rootstocks of different vigours. R ws prtitioned into soil root, soil stem, root stem, nd stem lef components, nd resistivity of stem sections with nd without grft unions ws mesured. Mterils nd methods Sites nd plnt mteril The experiments were in pple orchrds in Burlington, Vermont, USA nd in the highlnds of North-Estern Isrel (t Kibbutz Ortl). Detils of the different vrieties used re given in Tble 1, long with some informtion on their prentge, where vilble. Trunk cross-sectionl re nd totl lef re mesured on the trees in Vermont in 2002 re lso given. Trunk cross-sectionl res, which re used s reltive mesure of vigour, confirm tht the rootstock clssifiction ws roughly correct for conditions in northern Vermont. Ortl, Isrel: Mesurements were crried out in commercil fruitbering pple orchrd t Kibbutz Ortl (33 05#N; E; 900 m bove men se level) in North-Estern Isrel. Tree scions were of the Golden Delicious Smoothee cultivr on two rootstocks (MM106 nd virus-free M9), which in Isrel s climte produce Hydrulics nd rootstock vigour 4215 lrge nd medium sized cnopies, respectively, 3 yers fter plnting. Trees were plnted in 1997 nd trined s centrl leder. Irrigtion ws dily with n utomtic drip system, ccording to stndrd commercil prctice for the region. Trees were not pruned during the sesons when mesurements were mde. Mesurements were mde in rows of trees in which ll trees were of the sme rootstock. In ech seson, eight trees on both MM106 nd M9 rootstocks were mesured using two sp flow systems. Suckers, i.e. new shoots tht grew from the bse of the rootstock below the grft, were llowed to develop. Trees were selected for mesurement if they hd enough sucker leves for the mesurement progrmme. Burlington, USA: Mesurements were crried out in the University of Vermont s (UVM) horticulturl reserch centre in Burlington, VT (44 28#N; 73 9#W; 100 m bove men se level). Trees were from the NC Liberty/CG Apple Rootstock Tril led by Terence Robinson (see which, in Vermont, ws n evlution of severl M nd CG series rootstocks for the Cornell/Genev Rootstock Breeding Progrm with the scb-resistnt scion cultivr Liberty. Trees were plnted in 1992 in three rows, with ech row representing one of the types: dwrf, semi-dwrf, nd vigorous. The order of the rootstock vrieties vried t rndom long the row. For the current study, two typicl trees of ech of the following rootstocks were selected: vigorous M111 nd CG934, semi-dwrf M7A nd CG30, nd dwrf M9 nd CG202. This gve totl of 12 trees, but, due to sp flux instrumentl limittions, only eight were mesured simultneously. In order to mesure ll 12, the four trees on the vigorous rootstocks were lwys mesured, nd the dwrf nd semi-dwrf trees were mesured t different times. HPFM mesurements were mde on totl of eight of these trees in the utumn of 2002 (two M111s, one CG934, one M7A, one CG30, two M9s, nd one CG202). The orchrd ws rin-fed, since there is usully mple rin in the summer, nd supplementl irrigtion ws supplied with drippers. The summer of 2001 hd drought spell which overlpped with the mesurements, during which the orchrd ws not irrigted regulrly. The drought ws mild nd did not hve visible impct on yields. Mesurements were mde during the summers of 2001 nd Trees were not pruned during the two yers of the experiment. Orchrd mintennce included removl of suckers before they could be mesured. Tble 1. Descriptive prmeters of the rootstocks nd trees used in this study Ares re those of the Liberty scion mesured fter 11 yers, on trees in the rootstock tril in Vermont. For lef re mesurement, see the Mterils nd methods. Vriety Type Size clss Stem re, (m ) Lef re, (m 2 ) Prentge/Ltin nme M.9-EMLA Rootstock 3, dwrf Unknown b CG-202 Rootstock Dwrf M7 Rootstock 6, semi-dwrf Unknown, virus reduced clone b CG-30 Rootstock 5 6, semi-dwrf Robust 53M.9 MM.106-EMLA Rootstock 7, semi-vigorous N/A N/A Nothern Spy3M.1 b MM.111-EMLA Rootstock 8, vigorous Northern Spy3MI.793 b CG-934 Rootstock Vigorous Golden Delicious Scion N/A N/A N/A Mlus domestic Liberty Scion N/A N/A N/A Mlus domestic N/A not pplicble. b Source: Cornell University New York Stte Agriculturl Experimentl Reserch Sttion, Genev, NY fct sheet t: edu/hort/breeders/ppleroots/fctsheets/fsaccess.html. This web site, which contins dditionl informtion on the rootstocks, explins tht rootstocks re rnked by size clss from smllest (1) to lrgest (10). Size clsses re estimted s the reltive per cent tree size of n own-rooted (full sized) tree, e.g. size clss 1 represents rootstock tht produces tree 10 20% the size tht n own-rooted tree would produce under similr conditions. Downloded from

4 4216 Cohen et l. Sp flow Sp flow mesurements were mde with the het pulse technique (for detils see Cohen et l., 1981; Cohen, 1994) using custommde probes, heters, pulse genertors nd multiplexers (Ariel Amplifictions, Peth Tiqv, Isrel), nd commercil dtloggers (types CR21X nd CR10X; Cmpbell Scientific, Logn, UT, USA). Ech system consisted of eight heter nd probe pirs, one pulse genertor multiplexer, nd one dtlogger. The eight probe pirs were mesured sequentilly t 7.5 min intervls so tht ech probe pir ws mesured once per hour. Ech probe pir consisted of reference probe which mesured bckground spwood temperture ;10 cm below the heter, nd second probe 15 mm bove the heter, which contined six microbed thermistors, plced t 8 mm intervls long the probe length. The ltter probes nd the heters were inserted into holes drilled in the scion t lest 10 cm bove the grft, from the south of the tree. Sp flow ws mesured simultneously 4, 12, 20, 28, 36, nd 44 mm into the spwood. No consistent pttern in the zimuthl distribution of sp flux hs been found in the pst in pple trees (Cohen nd Nor, 2002). Clibrtion vlues nd prmeters for computing sp flux density were tken from previous work (Cohen et l., 1981; Jones et l., 1988; Cohen, 1994). Holes were drilled using precision-tooled guide to ensure tht heter nd probe bores were exctly 15 mm prt nd prllel for the full depth of the sensor probe. Distnces between probe nd heter for deep prts of the bores were checked severl times in nrrow (<6 cm dimeter) trunks where probe nd heter protruded from the opposite side of the trunk. In ll cses, the error in distnce ws <1 mm. Lef wter potentil W l W l ws mesured with pressure chmbers (PMS Instruments, Corvllis OR, USA nd Arimd, Kfr Hruv, Isrel). Leves were cut, immeditely bgged in plstic, nd then tken to the pressure chmber where they were shded until mesurement within few minutes. Covered leves, used for determintion of stem W, were covered with luminium foil either the previous evening or severl hours before mesurement (Nor, 1998). For mesurement of root W, ll leves of suckers were covered the previous dy, sucker shoots were shded with dense reflective shde screens, nd individul leves were mesured t middy. Covered leves were left in their covers until fter mesurement. Dily courses of W l used for computing hydrulic conductnce by the EF method strted with mesurements of pre-dwn W l, followed by either mesurement every 1 h or 1.5 h throughout the dy, or mesurements mde during 3 4 middy hours. Middy W tken for the R computtion ws the verge of the vlues for 3 h or 4 h when redings of both W nd sp flow were stble. Hydrulic conductnce evportive flux (EF) method In this method, flux is monitored together with W long the soil tree continuum, nd R is clculted s the rtio of W grdient to flux. R cn then be prtitioned into tht of the soil to root, root to stem, nd stem to lef pthwys (Moreshet et l., 1990; Clerwter et l., 2004). Pre-dwn W l (W pd ) ws tken s proxy for soil W (Cohen et l., 1983); lrge root W ws represented by the xylem W mesured on covered leves of the suckers (Simonneu nd Hbib, 1991); stem W ws mesured on covered leves selected inside the cnopy nd close to the min trunk bove the scion rootstock grft; nd W l ws tken s the verge mesured on equl numbers of exposed shded nd sunlit leves since wter flows in prllel to these two groups of leves (Moreshet et l., 1990). There re two possibilities for determining R (see Introduction): (i) W is tken s the chnge in W from before dwn to middy, nd the wter flux is tken s the verge obtined t middy; nd (ii) liner regression of hourly mesurements of W on wter flux. In order to decide which pproch to use, the reltionship of sp flow rte to stem W mesured t 1.5 h intervls from pre-dwn to lte fternoon on the sme tree on severl dtes ws exmined. Plots of W s function of sp flow showed tht there ws hysteresis in the dily curve. Therefore, when full dy of mesurements is not vilble, the regression pproch cn led to errors. However, for dys when most of the dy ws mesured t regulr intervls, the two pproches did not give significntly different results. The first pproch (i) ws dopted, which ws pplicble to ll the dt sets, nd it ws used to determine the EF R vlues reported here. Hydrulic conductnce high pressure flow meter (HPFM) method Mesurements of R using n HPFM (Tyree et l., 1995) were performed in Vermont, USA. Mesurements were with de-ionized, degssed wter with no dditives. Lrge pressure fittings were mnufctured to fit the tree trunks whose dimeters rnged from 4 cm to 10 cm. Holes in the trunk left from the sp flow mesurements were seled with screws nd rubber wshers to prevent leks. In order to get good sel, position on the trunk tht ws smooth, close to circulr in cross-section, nd did not hve holes from het pulse mesurements ws selected. These constrints resulted in differences in the length of trunk mesured on ech tree. The flow rte into the trunk t high pressure (;0.5 MP) ws in the order of 0.25 l min 1, so the HPFM ws fitted with 2 gllon (;8.0 l) cptive ir tnk, which ws refilled between mesurements. Trees were cut severl centimetres bove the grft union; the exposed wood of the trunk ws shved with rzor knife, nd then ttched to the HPFM. The upper prt of the tree (i.e. shoot) ws perfused through the trunk t high pressure until leves were visibly wterlogged, i.e. until leves becme drk green nd drops of wter were seen to exude from the stomt. This usully took less thn 30 min. At tht point R ws monitored until it becme stedy, nd qusi-stedy stte (QSS) reding ws tken (Boget-Triboulot et l., 2002). This ws followed by two or three trnsient mesurements. The HPFM ws then returned to stedy-stte mode nd ll leves were removed. The sme procedure (i.e. QSS nd trnsient mesurement) ws then repeted. The exposed lower prt of the trunk ws then shved nd ttched to the HPFM for root R mesurement. Attempts to mke immedite trnsient mesurements were unsuccessful becuse of non-linerity in the pressure flux plot. This is typicl problem when mesuring wood contining significnt mount of ir (Nrdini nd Tyree, 1999; Boget- Triboulot et l., 2002). The system ws then perfused until constnt R ws obtined (fter min) nd then QSS nd trnsient mesurements were mde. As differences between the QSS nd trnsient mesurements were not significnt, QSS mesurements re reported. Upon completion of the root mesurements, QSS mesurement continued while the trunk ws cut below the grft union. The trunk, which ws then cm long, ws subsequently shortened every few minutes by from 4 to 17 cm while QSS mesurement continued. Stem-specific resistivity of the stem section contining the grft union nd sections bove the grft tht belong to the scion were determined from the ltter mesurements. The length of the stem section contining the grft union verged 10 cm nd vried from 3 cm to 17 cm ccording to where it ws convenient to cut nd connect the HPFM fitting. In order to normlize the results, the length of the grft union ws tken s 5 cm nd, where the grft union stem section mesured exceeded 5 cm, R of section of scion stem of length equl to the excess length ws subtrcted from the result. HPFM mesurements were mde on one tree per dy, nd totl of eight trees were mesured (see Fig. 6). Mesurements begn in the morning between h nd h, nd took 2 3 h to complete. Downloded from

5 Lef re In the utumn or during HPFM mesurement (for trees mesured with the HPFM) ll leves were hrvested from the trees. These were weighed nd t lest three subsmples of t lest 100 g ech were tken for determintion of the rtio of lef re to fresh weight. Subsmple lef re ws determined with Li-Cor (model LI- 3100; Lincoln, NE, USA) nd Delt-T imge nlysis nd conveyor belt (Cmbridge, UK) lef re systems. The verge rtios were then used to determine totl lef re for ech tree. Sttistics Anlysis of vrince (ANOVA) ws with the GLM routine of SAS (SAS Institute, 1982) where rootstock, plce, nd yer were defined s clss vribles. Liner interctions between the clsses were tested. Differences between mens were considered significnt when type III sum of squres met the F-test criterion t <0.05 probbility. When ANOVA showed tht significnt differences existed between mens, the Duncn multiple rnge test (DMRT with ¼0.05) ws used to determine which mens were significntly different. Conductnce, conductivity, resistnce, nd resistivity Conductnce nd resistnce re reciprocls, nd express the wter trnsport bility of portion of the plnt irrespective of its length, in units of kg m 2 MP 1 s 1 nd MP m 2 s kg 1, respectively. Conductnce (nd resistnce) expressed reltive to lef re (K l nd R l ) nd cross-sectionl re of conductive tissue (i.e. specific conductnce) hve different implictions (Tyree nd Ewers, 1991; Tyree, 1999); the former expresses the bility of the plnt to supply wter to the leves, nd the ltter expresses the hydrulic bility of the stem. Conductivity nd resistivity (k nd r) re lso reciprocls, but these express the hydrulic properties of unit length of conductive tissue, with units of kg m 1 MP 1 s 1 nd MP m s kg 1, respectively. Since wter flux in the plnt, s mesured in this study, is through series of resistnces from soil to shllow roots to stem (nd through the grft union) to leves, the totl resistnce is the sum of the resistnces. It is therefore convenient to present the results s resistnce nd resistivity, nd when these re compred with vlues of conductnce previously reported, those dt hve been converted to resistnce. Determintion of the cross-sectionl re of conductive tissue is problemtic since the xylem my not be uniform, s indicted by the decrese of sp velocity with depth in trunks of pple trees (Cohen nd Nor, 2002). In the trees studied, sp velocity ws mesured to depth of 44 mm in the xylem, nd the reltionship of sp velocity to depth showed tht there ws no non-conductive hertwood. Therefore, conductnce ws not expressed reltive to conductive tissue but reltive to trunk (i.e. stem) cross-sectionl re. This is referred to s stem-specific conductnce nd its inverse, resistnce (K s nd R s ). Hydrulics nd rootstock vigour 4217 rootstocks. During the summer of 2002, W pd ws higher nd R s,soil stem remined reltively low. Since for the dry conditions of 2001 soil to stem nd totl R were more influenced by soil wter thn rootstocks, they re not reported. Stem- (R s, Fig. 1A) nd lef- (R l, Fig. 1B) specific resistnce of the soil to stem pthwy of three rootstocks, M9, MM106, nd MM111, were mesured in both countries during two summers (Fig. 1) nd dditionl dt for the Isreli site re vilble from previous study (Tble 2). Becuse of the similrity between MM106 nd MM111 in both genetics nd vigour (Tble 1), they re presented s comprison with the dwrfing M9 rootstock. Significnt differences between rootstocks for R s,soil stem (Fig. 1A) were not found in ny of the cses, while men R l,soil stem (Fig. 1B) ws consistently greter in M9, significntly so in Isrel in Significnt differences were found between the sites nd yers of mesurement; R s,soil stem rnged from 6.1 to 17.2, nd R l,soil stem from to MP m 2 skg 1. Root to stem resistnce EF method R root stem is the sum of the xil root R from the point of mesurement in the lrge roots (i.e. where the sucker grew out of the root) to the stem, nd tht of the stem nd the Results Soil to stem resistnce EF method R soil stem is the sum of the soil resistnce t the soil root interfce, rdil nd xil resistnces in the root, nd resistnce of the stem, including the rootstock scion union. During the drought in the summer of 2001 in Vermont, R s,soil stem incresed s W pd decresed, pprently due to the incresingly lrge R of the drying soil. The increses exceeded the differences between Fig. 1. Stem- (A) nd lef- (B) specific EF hydrulic resistnce for the soil to scion stem pthwy. Mesurements re for the dwrf M9 nd the vigorous MM106 (Isrel) nd MM111 (Vermont) rootstocks during three summers. Verticl brs indicte 6SEM. ANOVA for ech set of dt indicted significnt differences between rootstocks (P <0.01). Letters indicte significnt clsses from DMRT (P <0.05). Downloded from

6 4218 Cohen et l. Tble 2. Stem- nd lef-specific hydrulic resistnce (s MP m 2 kg 1, men 6SE) mesured by the EF method during the experiment Numbers with the sme letter re not significntly different t ¼5% (DMRT). Levels of significnce (P >F) re from ANOVA. Plce Yer Clss Rootstock R s, soil stem R l, soil stem R s, stem lef R l, stem lef Soil stem/ Soil lef Isrel 2002 Dwrf M Isrel 2004 Dwrf M cd bcd Isrel c 1998 Dwrf M Vermont 2001 Dwrf M cd bc Vermont 2002 Dwrf M cd bcd cd c 0.74 Vermont 2001 Dwrf CG bc Vermont 2002 Dwrf CG d bcd cd b 0.68 Vermont 2001 Semi-dwrf M bc Vermont 2002 Semi-dwrf M d bcd bc bc 0.64 Vermont 2001 Semi-dwrf CG d bc Vermont 2002 Semi-dwrf CG d bc bc Isrel 2002 Semi-dwrf MM b b Isrel 2004 Semi-dwrf MM d d Isrel c 1998 Semi-dwrf MM Vermont 2001 Vigorous MM bc bc Vermont 2002 Vigorous MM cd cd bc bc 0.66 Vermont 2001 Vigorous CG Vermont 2002 Vigorous CG bc bcd b bc 0.72 Significnce (P >F) All <0.001 <0.001 <0.001 <0.001 Rootstock <0.05 <0.05 <0.001 <0.001 Plce <0.001 <0.001 b b Yer <0.001 <0.001 n.s. <0.001 Rootstock3plce n.s. n.s. b b Rootstock3yer b b <0.01 <0.001 Dt for the soil to stem pthwy mesured in Vermont in 2001 hve been omitted. See text. b Not pplicble. c Dt mesured in different orchrd on the sme Kibbutz. EF methodology ws the sme but lef re ws determined by gp frction inversion, so R l is not included. For detils see Cohen nd Nor (2002). These dt were not included in the sttisticl nlysis. grft union. These mesurements (Fig. 2A, B) were mde in M9 nd MM106 during two summers in Isrel. In both cses, R root stem in M9 ws higher, but lrge differences were observed for M9 in the two summers, with the vlue for 2002 being >4 times tht observed in For MM106, vlues obtined in the two summers were not significntly different, nd R s,root stem nd R l,root stem verged 1.0 nd 2000 s MP m 2 kg 1, respectively. R root stem represented 13 22% of R soil stem for MM106 nd 30 45% for M9 (Fig. 2C). Thus, in these wellwtered situtions, R through the root nd cross the grft union for M9 is comprble in mgnitude with R from the soil to the lrge-root xylem. Stem to lef resistnce EF method R s nd R l from stem to lef for the six rootstocks ws mesured in two summers in Vermont (Fig. 3A, B). Mesurements mde in Isrel in 1998 in previous study (Cohen nd Nor, 2002) gve results similr to those from Vermont, nd re given here for comprison (Tble 2). Significnt differences were found between rootstocks nd between the yers (Tble 2), but the only trend observed ws significnt positive correltion between R s,stem lef nd rootstock vigour (Fig. 3A). The lowest R s,stem lef ws found for the semi-dwrf, CG30, nd the highest for the lrgest (nd most vigorous) trees, CG934. The pooled reltionship between R s,stem lef nd trunk cross-sectionl re re (A in m 2, Fig. 3C) for the two yers ws R s,stem lef ¼ 369 A+1.96 (r 2 ¼0.54; P <0.01). For the soil to stem nd totl soil to lef pthwys, mesured in 2002, R s ws lso significntly (P <0.05) positively correlted with scion trunk cross-sectionl re (Fig. 4) nd not with tree lef re. No significnt reltionships were found between vigour nd R l for ny of the pthwys. The rtio of resistnce in the soil stem to the stem lef pthwy rnged from 0.52 to 0.74 (Tble 2). The rtio ws not significntly relted to the vigour ctegories. HPFM mesurements HPFM mesurements were used to determine R l (Fig. 5A) nd percentge of R (Fig. 5B) for the different prts of the tree for ech of the rootstocks, where results re from either one individul tree or n verge of two trees. In ll cses the prt of the stem contining the grft union comprised only smll prt of the resistnce to wter flow. As expected, the highest R occurred in the root system, which constituted pproximtely hlf of the totl R, nd the combined R of stem nd leves ws comprble. Similrly, Lndsberg et l. (1976) reported tht root resistnce ccounted for 40 74% of the totl Downloded from

7 Hydrulics nd rootstock vigour 4219 Fig. 2. Lef- nd stem-specific EF hydrulic resistnce from root to scion stem (A, B), nd expressed s percentge of the totl resistnce from soil to scion stem (C) for M9 nd MM106 mesured in Isrel during two summers. Verticl brs indicte 6SEM. ANOVA for ech set of dt indicted significnt differences between rootstocks (for A nd C, P <0.05; for B, P <0.01). Letters indicte significnt clsses from DMRT (P <0.05). plnt resistnce in young pple trees. In the present cse, the lef R includes tht of the petioles, since the leves were removed t the bse of the petioles. Prtitioning of R between the four tree prts did not revel ny cler reltionship with rootstock vigour clss. EF nd HPFM mesurements mde on the sme trees were compred for the lower (root stem) nd upper (stem lef) prts of the tree (Fig. 6A, B). In ll except one cse (i.e. the shoot of CG934), EF R ws much higher thn tht obtined with the HPFM. The verge rtios of HPFM to EF vlues of R were 0.42 nd 0.59 for the lower nd upper prts of the tree, respectively. No correltion between the rtios nd rootstock vigour ws pprent. Resistivity of grft union nd non-grft union trunk sections ws determined for six stems. In dwrf trees, lefspecific resistivity of the grft (Fig. 7) ws severl times Fig. 3. Stem- (A, B) nd lef- (C) specific hydrulic EF resistnce mesured for the scion stem to lef pthwy. Mesurements from the Vermont rootstock tril during two summers. Resistnce is plotted for ech rootstock (A, C), nd s function of reltive stem cross-sectionl re (B). Verticl brs indicte 6SEM. ANOVA for ech set of dt indicted significnt differences between rootstocks (P <0.01). Letters indicte significnt clsses from DMRT (P <0.05). tht of the scion stem, in the semi-dwrfs grft union nd scion hd similr resistivity, nd in the one vigorous tree resistivity of the grft union ws much lower thn tht of scion stem. Resistivity of the scion stem sections ws not significntly different on different rootstocks. Downloded from

8 4220 Cohen et l. Fig. 4. Stem- (A) nd lef- (B) specific hydrulic EF resistnce mesured for the soil to scion stem nd full soil to lef pthwy. Mesurements from the Vermont rootstock tril in Resistnce is the verge for ech rootstock. Verticl brs indicte 6SEM of two trees mesured on two dys. ANOVA for ech set of dt indicted significnt differences between rootstocks (P <0.01). Letters indicte clsses from DMRT (P <0.05). Discussion Accurcy nd precision of EF mesurements of hydrulic resistnce EF R is derived from mesurements of lef wter potentil, sp flow rte, nd lef re or trunk crosssectionl re. The errors in ech of these prmeters my dd up. The lest ccurte re sp flow rte nd lef re. Lef re meter mesurements re ccurte to 3%, while the use of the reltionship between subsmple wet weight nd re introduces nother error of the sme mgnitude, bsed on stndrd errors of the subsmples, giving n estimted ccurcy of 5 10% for individul tree lef re. The het pulse technique, s implemented in this study, gives ccurte mesurements of sp flux density (Cohen, 1994) nd compred fvourbly with n open chmber method in pple trees (Drgoni et l., 2005). One source of error, i.e. tht due to inccurcy of the distnce between heter nd probe (Jones et l., 1988), ws minimized here with the use of drill guide tht gve ccurte bores for the full probe length (see Mterils nd methods). The Fig. 5. Lef-specific (A) nd percentge (B) resistnce in the different prts of the tree, from HPFM mesurements of full-sized 11-yer-old trees from the Vermont rootstock tril. Semi, semi-dwrf; vigor, vigorous. n¼1. physicl properties of the wood influence het pulse mesurements. However, since ll sp flow mesurements in the current study were mde in wood of the scion Golden Delicious vriety in Isrel nd the Liberty vriety in Vermont, differences in therml trnsport properties of the wood re unlikely to hve introduced bis in the results when compring results within ech country. Sp flux density is highly vrible from tree to tree, nd cn lso vry depending on the zimuth t which the probe is inserted in the trunk (Cohen nd Nor, 2002; Drgoni et l., 2005). Cohen (1991) found the coefficient of vrition (CV) for mesurements in different citrus trees in the sme tretment to be 0.3. In the present cse, since the mesurements were verges of 2 8 trees per vigour (in Vermont nd Isrel, respectively), the ccurcy of sp flow is probbly not better thn 15%. Summing these two errors gives n estimte of ;25% for the ccurcy of verge of lef-specific R estimted by the EF method in this study. In the summer of 2001, four trees, two M111 nd two CG934, were mesured on four dys. The vribility in these mesurements cn give n indiction of the precision of the EF mesurements. R in the soil to stem nd stem to lef pthwys ws determined independently for Downloded from

9 Hydrulics nd rootstock vigour 4221 Fig. 7. HPFM mesurements of lef-specific stem resistivity for grft union nd scion. Mesurements were mde on sections of the min trunk of individul fully grown trees. Rootstock type nd tree ID re given. Where n >1, verticl brs indicte 6SEM. Fig. 6. (A) Comprison between totl plnt stem-specific hydrulic resistnce mesured by the EF nd HPFM methods on eight trees from the Vermont rootstock tril in 2002 (n¼1). Rootstock type is indicted. (B) Rtio of HPFM (QSS) to EF mesurements of hydrulic resistnce for the soil stem nd stem lef pthwys. Dt points were computed from mesurements mde on the individul trees tht were hrvested in the utumn of Size clss, tree seril ID, nd rootstock re noted. Semi, semi-dwrf; vigor, vigorous. ech of the dys. The verge CV for the four dy verges for the four trees ws 2561% nd 2565%, for the soil to stem nd stem to lef pthwys, respectively. The CV for the verges of the two yers of mesurement of R from stem to leves for M9 ws 11% (Tble 2). It is therefore expected tht the CV for mesurement of R with the EF technique used in this study is between 10% nd 25% nd, since dt presented re usully n verge of 2 4 mesurements, their confidence intervl is in the order of 10% of the men. Mgnitude of hydrulic resistnce nd resistivity comprison with other reports for pple Severl studies hve reported hydrulic dt for pple trees tht, fter mnipultion, cn be compred with the present mesurements. Cohen nd Nor (2002; Tbles 2, 3) used the sme EF method during one summer (1998) nd reported vlues of similr mgnitude. The current study improves on tht previous one in tht more replicte mesurements were mde (i.e. two sesons in Isrel nd two in the USA), nd lef re mesurement here ws mesured directly, while the previous study used gp frction nlysis, whose ccurcy is only ;20% (Welles nd Cohen, 1996; Cohen et l., 1997) nd cn be influenced by cnopy clumpiness, which my not be constnt from tree to tree (Cohen et l., 1995). R s components for full-sized orchrd-grown Cox s Ornge Pippin tree (Tble 3), reported by Lndsberg et l. (1976), were close to the present vlues (Tble 2; Figs 3, 4), but R l vlues were n order of mgnitude lower. Their experiment ws performed in October, nd lthough they noted tht it ws before lef fll, the lef re my well hve been less thn during the min growing seson. Components of R l for 2-yer-old potted trees of the Golden Delicious vriety (Lndsberg et l., 1976; Tble 3) were n order of mgnitude higher thn those in the present study. There is evidence tht under low evportive demnd when wter supply is not limiting fctor, lef-specific hydrulic resistnce cn be higher thn when wter supply is limiting (Li et l., 2005). It is suggested tht in the ltter study, the potted trees might hve been grown in such conditions, leding to high lef-specific resistnce. Atkinson et l. (2003) mesured in vitro conductivity (i.e. conductnce per unit length) t low pressure (6 kp) of sections of root nd stem cut under wter for three pple rootstocks from grfted nd ungrfted trees. Their results, converted to lef-specific resistivity, for scion stem (which rnged from 970 to 1900 s MP m kg 1 ) nd the grft union ( s MP m kg 1 ) re close to the present HPFM mesurements (Fig. 7). They lso found through stining tht only frction of the stem is ctive in wter trnsport. The ltter, together with the fct tht the present in vivo mesurements of R were higher thn those mde t high pressure (Fig. 6b), suggests tht significnt portion of the xylem in the trees under study here my hve been dysfunctionl, possibly due to Downloded from

10 4222 Cohen et l. Tble 3. Comprison of pple stem- nd lef-specific hydrulic resistnce (s MP m 2 kg 1 ) vlues mesured with similr EF methodology Source Species or pple vriety Rootstock R s, soil stem R l, soil stem R s, stem lef R l, stem lef Current study See Tble Cohen nd Nor (2002) Apple Golden Delicious M MM Lndsberg et l. (1976) Apple Cox s Ornge Pippin yers old 2-yer-old potted trees cvittion. However, if cvittion is significnt, then their mesurements t low pressure, t which refilling of cvitted vessels is not believed to occur (Sperry et l., 1988), should hve given higher resistnce thn the present HPFM mesurements. Tht ws not the cse. Atkinson et l. (2003) lso reported tht stining ws less in the scion stem of two dwrfs thn in the more vigorous MM106, which might be tken s n indiction of more xylem dysfunction. The ltter is not supported by the rtios of in vivo high pressure to in vitro conductnce shown in Fig. 6B. They concluded tht stem-specific R ws higher in dwrfs, while the present in vivo mesurements show significnt decrese with decresing vigour (Figs 3, 4). One importnt difference from Atkinson et l. (2003) is tht they mesured young stems, while fully grown tree stems were mesured in the present study. Since for the ltter, stem cross-sectionl re is highly positively correlted with vigour (nd is ctully used s mesure of vigour), the correltion of vigour with stem-specific R my indicte tht smller percentge of the stem is ctive in the vigorous trees with the lrge stems. When trees re young nd stem cross-sectionl re of the different rootstocks is more similr, s my hve been the cse for Atkinson et l. (2003), the sitution my be different. Rootstock hydrulic resistnce comprisons with other species Nrdini et l. (2006) reported HPFM mesurements of R for dwrf nd vigorous selections of one olive cultivr, Ole europ cv. Leccino. Grfted nd non-grfted 3- yer-old splings 360 d nd 450 d fter grfting were mesured. They found tht the smller root systems of the dwrf splings hd significntly higher resistnce thn those of the more vigorous splings, but when root resistnce ws expressed reltive to the lef re (i.e. s R l ) differences between vigours were smll. Their vlues of R l,root stem not including the grft rnged from 8000 to s MP m 2 kg 1 nd of R l,stem lef including the grft rnged from 3000 to s MP m 2 kg 1. These vlues re very close to the present vlues (Fig. 5A). Bsile et l. (2003, b) reported HPFM mesurements of pech trees on three rootstocks of different vigours. Their mesurements gve R l,root stem vlues of s MP m 2 kg 1 nd R l,stem lef vlues of s MP m 2 kg 1, which is lso within the rnge of the present mesurements. They found tht diurnl chnges in stem wter potentil nd differences in lef-specific R of the root nd grft system were negtively correlted with differences in shoot elongtion rtes. The differences in R tht they observed were of the order of 22 26%, which is smller thn the 95% confidence intervls (i.e. 2 SEMs) for some of the mens mesured in the current study. Evlution of the ccurcy nd precision of the EF mesurements of resistnce (see bove) indictes tht if differences in R between pple rootstocks were greter thn 20%, s found by Bsile et l. (2003, b) in pech trees, it would hve been expected to hve found them in the current study, nd this ws not the cse. Differences between HPFM nd EF mesurements HPFM mesurements of R were significntly lower thn those for the EF method in lmost ll cses (Fig. 6). For the root system, where pprent ir in the wood prevented mesurements of R until fter perfusion, higher vlues of R might be expected due to ccumultion of ions in the roots during perfusion (Tyree et l., 1995). However, for the roots, the HPFM still gve lower vlues thn the EF method (Fig. 7). Tsud nd Tyree (2000) mde extensive comprisons between the EF nd HPFM methods for nnul plnts nd smll tree brnches nd found tht results re usully similr, but Rieger (1989) found tht, in pech, high pressure mesurements sometimes gve significntly lower resistnce thn low pressure mesurements. He hypothesized tht the difference cn be n indiction of xylem dysfunction due to cvittion in the xylem. The ir-filled xylem is rehydrted under high pressure, thus cusing the decresed resistnce. It is ssumed tht in the lrge trees mesured in the current study the discrepncy between the HPFM nd EF mesurements (Fig. 6) cn be explined in this wy. R nd rootstock vigour Of the four sets of EF mesurements, only one, tht for Isrel in 2002, supports previous findings (Cohen nd Nor, 2002; Atkinson et l., 2003) tht lef-specific R in the soil to scion stem pthwy for trees on the dwrf M9 Downloded from

11 rootstock is significntly higher thn tht for more vigorous MM106 nd MM111 rootstocks (Tble 2; Figs 1B, 6B), especilly for the pthwy from lrge roots to scion stem (Fig. 2B). For the other dt sets, nd from lrger set of six rootstocks of different vigours (Fig. 4), some significnt differences in resistnce were found, but there ws no consistent negtive reltionship between rootstock vigour nd R, whether on lef-specific or stemspecific bsis. Severl HPFM mesurements of R did not show ny other ptterns, but mesurements of stem sections with nd without grft unions showed tht resistivity of the grft union is lrger t lower vigour. Resistnce of the grft union comprised only smll prt of the totl plnt R. Therefore, it is concluded tht vritions in totl lef- or stem-specific hydrulic resistnce cnnot be the only explntion for the differences in observed vigour of the pple rootstocks. Conclusions Exmintion of series of mture pple trees on rootstocks with rnge of vigours indicted tht stem- nd lef-specific R in the soil to stem, stem to lef, nd totl soil to lef pthwy were not consistently negtively correlted with vigour. The only consistent grdient in hydrulics observed ws n increse in stem-specific R (i.e. decrese in conductnce) with incresing vigour (Figs 3A, C, 4A). R differences between rootstocks were smller thn those cused by indequte irrigtion. Even so, the resistivity of grft union portions of the stem ws found to decrese with incresing vigour (Fig. 7). This my influence the trnsport of wter nd other elements cross the grft union, nd my therefore be involved in the dwrfing mechnism. Acknowledgements Thnks to Drs Aln Lkso nd Terence Robinson for helpful discussions, to Dr Elen Grci nd the stff of the University of Vermont s Horticulturl Reserch Center in Burlington for ccess to nd mintennce of the Vermont 1992 NC-140 rootstock tril which included some of the trees used in this study. Thnks to Victor Lukynov nd the stff of MIGAL, Kiryt Shmon for help with the mesurements in Isrel, nd to Kibbutz Ortl for ccess to their orchrds t Ortl nd Dlowy. For technicl ssistnce thnks to Dr F Li in Isrel nd to A Rye nd the stff of the Aiken Forestry lbortory in Burlington. This reserch ws supported by Reserch Grnt Awrd no. IS from BARD, The United Sttes Isrel Bintionl Agriculturl Reserch nd Development Fund, nd by grnt number from the Chief Scientist of the Isreli Ministry of Agriculture. Contribution from the Agriculturl Reserch Orgniztion, Institute of Soil, Wter nd Environmentl Sciences, Bet Dgn, Isrel No. 607/05. References Atkinson CJ, Else MA, Tylor L, Dover CJ Root nd stem hydrulic conductivity s determinnts of growth potentil in Hydrulics nd rootstock vigour 4223 grfted trees of pple (Mlus pumil Mill.). Journl of Experimentl Botny 54, Bsile B, Mrsl J, Dejong TM Dily shoot extension growth of pech trees growing on rootstocks tht reduce scion growth is relted to dily dynmics of stem wter potentil. Tree Physiology 23, Bsile B, Mrsl J, Solri LI, Tyree MT, Bryl BR, Dejong TM. 2003b. Hydrulic conductnce of pech trees on rootstocks with differing size-controlling potentils. Journl of Horticulturl Science nd Biotechnology 78, Bermn ME, Dejong TM Diurnl ptterns of stem extension growth in pech (Prunus persic): temperture nd fluctutions in wter sttus determine growth rte. Physiologi Plntrum 100, Boget-Triboulot M-B, Mrtin R, Chtelet D, Cochrd H Hydrulic conductnce of root nd shoot mesured with the trnsient nd dynmic modes of the high-pressure flowmeter. Annls of Forest Science 59, Clerwter MJ, Lowe RG, Hofstee BJ, Brcly C, Mndemker AJ, Blttmnn P Hydrulic conductnce nd rootstock effects in grfted vines of kiwifruit. Journl of Experimentl Botny 55, Clerwter MJ, Seleznyov AN, Thorp TG, Blttmnn P, Brnett AM, Lowe RG, Austin PT Vigor-controlling rootstocks ffect erly shoot growth nd lef re development of kiwifruit. Tree Physiology 26, Cohen S, Mosoni P, Meron M Cnopy clumpiness nd rdition penetrtion in young hedgerow pple orchrd. Agriculturl nd Forest Meteorology 76, Cohen S, Nor A The effect of three rootstocks on wter use, cnopy conductnce nd hydrulic prmeters of pple trees; nd predicting cnopy from hydrulic conductnce. Plnt, Cell nd Environment 25, Cohen S, Sudhkr Ro R, Cohen Y Cnopy trnsmittnce inversion using line quntum probe for row crop. Agriculturl nd Forest Meteorology 86, Cohen S, Tyree MT, Nor A, Lkso AN, Robinson TL Influence of hydrulic properties of rootstocks nd the rootstockscion grft on wter use nd productivity of pple trees Finl report of BARD project no. IS Cohen Y Determintion of orchrd wter requirement by combined trunk sp flow nd meteorologicl pproch. Irrigtion Science 12, Cohen Y Thermoelectric methods for mesurement of sp flow in plnts. Advnces in Bioclimtology 3, Cohen Y, Fuchs M, Cohen S Resistnce to wter uptke in mture citrus tree. Journl of Experimentl Botny 34, Cohen Y, Fuchs M, Green GC Improvement of the het pulse method for determining sp flow in trees. Plnt, Cell nd Environment 4, Dvid TS, Ferreir MI, Cohen S, Pereir JS, Dvid JS Constrints on trnspirtion from n evergreen ok tree in southern Portugl. Agriculturl nd Forest Meteorology 122, Drgoni D, Lkso AN, Piccioni RM Trnspirtion of pple trees in humid climte using het pulse sp flow guges clibrted with whole-cnopy gs exchnge chmbers. Agriculturl nd Forest Meteorology 130, Gsco A, Nrdini A, Rimondo F, Gortn E, Motisi A, Lo Gullo MA, Slleo S Hydrulic kinetics of the grft union in different Ole europe L. scion/rootstock combintions. Environmentl nd Experimentl Botny 60, Higgs KH, Jones HG Response of pple rootstocks to irrigtion in south-est Englnd. Journl of Horticulturl Science 65, Downloded from

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